iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
The origin of vertebrates
Marc Kirschner
Dept. of Systems Biology
Harvard Medical School
Boston Massachusetts
Plan of Lecture
• Introduction: Vertebrate
body plans and the odd
phylum of Hemichordates
• The origin of the vertebrate
nervous system: the
hemichordate perspective
Plan of Lecture
• Telling the back from the
front and what the
chordates invented
• How the vertebrates got
their chord
The American Society for Cell Biology
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
What do we vertebrates have in common?
How did these features arise in evolution?
Fundamentally, what we have
in common is a body plan
Anterior
Posterior
Fundamentally, what we have
in common is a body plan
Anterior
Right
Left
Dorsal
Ventral
Posterior
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
But body plans are shared
with many metazoan phyla
Mollusk
Arthropod
Rotifer
Flatworm
What makes our phylum, the
Chordates, special?
Dorsal
Ventral
Why study hemichordates?
Not many good choices
Includes
Urochordates and
Cephalochordates
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
To understand the Chordate origins, we
need to step back from Chordates
• If we are too far, eg. flies, we
cannot find the traces of the
chordate developmental
characters
• If we are too close, eg. within
sea squirts, then all we see is
the elaboration of these
characters
Echinoderms are too weird to inform
us about vertebrate body plans
Class: Crinoids; sea lilies
Class: Ophiuroids; brittle stars
Class: Asteroids; starfish
Class: Echinoids; sea urchins
Class: Holothuroids; sea cucumbers
Enter the hemichordates and their not
Hemichordate body plan
so obvious similarities with chordates
The American Society for Cell Biology
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
Enter the hemichordates and their not
Hemichordate body plan
so obvious similarities with chordates
Enter the hemichordates and their not
Hemichordate body plan
so obvious similarities with chordates
As we shall see, only one of these, gill slits are real homologies
The object of study: the Acorn Worm:
Saccoglossus kowalevskii
Metasome (pharynx, gut)
Mesosome
(collar)
Prosome
(proboscis)
1 cm
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iBioSeminars: Marc Kirschner, March 2008
S. kowalevskii - deuterostome development
The Origin of Vertebrates, Part 1
Eggs spawned in the burrows
Encapsulated throughout early development
Saccoglossus kowalevskii: the research lineage
Alexander
Kowalevsky
1867
William Bateson
1884-1886
T.H. Morgan
1894-1896
Woods Hole MA, 1999-present
Theodore
Bullock
UC Berkeley
PhD 1946
Laura Colwin
Arthur Colwin
Woods Hole MA,
1952-1962
Is this the moment
for the
hemichordates to
make their big
contribution?
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
Part 1. The origin of the
vertebrate nervous system
Marc Kirschner
Dept. of Systems Biology
Harvard Medical School
Boston Massachusetts
The long history of hypotheses on chordate
origins focus on the origin of the vertebrate
nervous system
The classical hypotheses can be basically divided into two groups - one that
reconstructs the ancestor of chordates to a larval life history stage on one that derives
chordates from adults.
Garstang was very influencial and formed the inspriation for a entire school of thought
people like Berrill.
Many of these hypotheses are based on the derivation of nervous system.
Drosophila CNS
Ventral side
Human CNS
Dorsal side
Theories of chordate origins:
mostly of historical interest
The American Society for Cell Biology
As a common ancestor for the deuterostome phyla echinoderms (sea urchins and star
fish), enteropneusts (hemichordates: acorn worms) and chordates (tunicates, lancelets
and vertebrates) Garstang proposed an ancestor resembling an auricularia type
echinoderm larva The auricularia possesses a ciliated ring, directly underlain by a
nerve cord. This ciliated ring separates an aboral and an oral epithelial region. During
the evolution of the chordate branch, the ciliated ring would shift dorsally and fuse in
the mid-dorsal region. The ciliated ring of the auricularia would be homologous to the
vertebrate neural ridges. The aboral epithelial field, internalised if the neural ridges
fuse, were to evolve into the neural plate. Evidence for this view was found in
comparative microscopic anatomy studies between echinoderms, hemichordates and
amphioxus. Ultrastructural correspondences were found between the so-called
multipolar cells -- part of the larval ciliated band -- of the studied echinoderm and
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
Due to molecular studies this
bizarre one is of great interest
Our experimental strategy
•Find the worms
•Work out the early embryology
•Identify interesting genes
•Examine gene expression
•Design RNAi experiments
•Interpret the results
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
The organization of the
nervous system in
Saccoglossus is
nothing like vertebrates
or insects
It is a diffuse nerve net
Dorsal and ventral cords are axon tracks
We have been focusing on nervous system organization as the two cords have been
variously proposed as the homologue of the chordate dorsal nerve cord.
E. Knight-Jones
1952
The nerve cells are not localized but
symmetrical around the body
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
Early neuronal markers
are distributed
symmetrically
Despite the fact that Saccoglossus has no
CNS, the patterning genes are expressed in
the same pattern as they are in the
vertebrate forebrain
Mouse
brain
early
late
development development
Though it has no fore or mid brain the
geographical markers are there
The American Society for Cell Biology
Notice a marked shift in the posterior limit of expression of this group of genes in
hemichordates.
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
For Hox gene expression in more posterior
regions the homologies persist
A conserved domain
map in
Hemichordates and
Vertebrates
Important signaling
centers are conservedeg. the vertebrate
midbrain-hindbrain
boundary in a brainless
hemichordate
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
The remarkable ancestry of the midbrain-hindbrain boundary
(primarily
vertebrate)
The hemichordate pattern is more vertebrate-like than
amphioxus or ascidians. Yet the hemichordate has
nothing resembling a midbrain or hindbrain…
Conclusions
• Conservation of transcriptional pattern
despite the fundamental organizational
differences
• Patterning genes are not reliable markers
of any specific neuroanatomical
organization
• Much of the regulatory networks involved
in vertebrate brain regionalization were
established early in deuterostome history.
• Nerve nets may be complex
Are we correct to
think that a
decentralized nervous
system was the
ancestral state?
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iBioSeminars: Marc Kirschner, March 2008
The Origin of Vertebrates, Part 1
Or did centralization occur once in an
early ancestor and did the vertebrates
merely shift the dorsal/ventral axis?
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